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Proc Natl Acad Sci U S A. 2019 Nov 5;116(45):22833-22843. doi: 10.1073/pnas.1913575116. Epub 2019 Oct 21.

Corticobasal ganglia projecting neurons are required for juvenile vocal learning but not for adult vocal plasticity in songbirds.

Author information

1
Graduate School of Life Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan.
2
Faculty of Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan.
3
Department of Structure and Function of Neural Networks, Korea Brain Research Institute, Daegu 41068, South Korea.
4
Department of Cognitive and Behavioral Sciences, The University of Tokyo, Meguro, Tokyo 153-8902, Japan.
5
Department of Brain Development and Neural Regeneration, Tokyo Metropolitan Institute of Medical Science, Setagaya, Tokyo 156-8506, Japan.
6
Center for Genetic Analysis of Behavior, National Institute for Physiological Sciences, Okazaki, Aichi 444-8585, Japan.
7
Graduate School of Life Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan; wada@sci.hokudai.ac.jp.
8
Department of Biological Sciences, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan.

Abstract

Birdsong, like human speech, consists of a sequence of temporally precise movements acquired through vocal learning. The learning of such sequential vocalizations depends on the neural function of the motor cortex and basal ganglia. However, it is unknown how the connections between cortical and basal ganglia components contribute to vocal motor skill learning, as mammalian motor cortices serve multiple types of motor action and most experimentally tractable animals do not exhibit vocal learning. Here, we leveraged the zebra finch, a songbird, as an animal model to explore the function of the connectivity between cortex-like (HVC) and basal ganglia (area X), connected by HVC(X) projection neurons with temporally precise firing during singing. By specifically ablating HVC(X) neurons, juvenile zebra finches failed to copy tutored syllable acoustics and developed temporally unstable songs with less sequence consistency. In contrast, HVC(X)-ablated adults did not alter their learned song structure, but generated acoustic fluctuations and responded to auditory feedback disruption by the introduction of song deterioration, as did normal adults. These results indicate that the corticobasal ganglia input is important for learning the acoustic and temporal aspects of song structure, but not for generating vocal fluctuations that contribute to the maintenance of an already learned vocal pattern.

KEYWORDS:

critical period; sensorimotor learning; sensory feedback; time-locked firing; zebra finch

PMID:
31636217
DOI:
10.1073/pnas.1913575116

Conflict of interest statement

The authors declare no competing interest.

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